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Flycatcher Song in Allopatry and Sympatry – Convergence, Divergence and Reinforcement

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Flycatcher Song in Allopatry and Sympatry – Convergence, Divergence and Reinforcement doi:10.1111/j.1420-9101.2003.00682.x Flycatcher song in allopatry and sympatry – convergence, divergence and reinforcement J. HAAVIE,* T. BORGE,* S. BURES,à L. Z. GARAMSZEGI,§ H. M. LAMPE, J. MORENO,– A. QVARNSTRO¨ M,** J. TO¨ RO¨ K & G.-P. SÆTRE* *Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden Department of Biology, University of Oslo, Oslo, Norway àLaboratory of Ornithology, Palacky University, Olomouc, Czech Republic §Department of Biology, Universitaire Instelling Antwerpen, Wilrijk, Belgium –Departamento de Ecologı´a Evolutiva, Museo Nacional de Ciencias Naturales, Madrid, Spain **Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eo¨tvo¨s University, Budapest, Hungary Keywords: Abstract cultural inheritance; The theory of reinforcement predicts that natural selection against the Ficedula; production of unfit hybrids favours traits that increase assortative mating. hybridization; Whether culturally inherited traits, such as bird song, can increase assortative reinforcement; mating by reinforcement is largely unknown. We compared songs of pied song; (Ficedula hypoleuca) and collared flycatchers (F. albicollis) from two hybrid species recognition. zones of different ages with songs from allopatric populations. Previously, a character divergence in male plumage traits has been shown to reinforce premating isolation in sympatric flycatchers. In contrast, we find that the song of the pied flycatcher has converged towards that of the collared flycatcher (mixed singing). However, a corresponding divergence in the collared flycatcher shows that the species differences in song characters are maintained in sympatry. Genetic analyses suggest that mixed song is not caused by introgression from the collared flycatcher, but rather due to heterospecific copying. Circumstantial evidence suggests that mixed song may increase the rate of maladaptive hybridization. In the oldest hybrid zone where reinforce- ment on plumage traits is most pronounced, the frequency of mixed singing and hybridization is also lowest. Thus, we suggest that reinforcement has reduced the frequency of mixed singing in the pied flycatcher and caused a divergence in the song of the collared flycatcher. Whether a culturally inherited trait promotes or opposes speciation in sympatry may depend on its plasticity. The degree of plasticity may be genetically determined and accordingly under selection by reinforcement. Introduction population will mix (introgression) and over time the populations will blend. However, if the hybrids have low When two populations come into secondary contact they fitness, natural selection will favour traits that increase may have diverged to such an extent that they do not assortative mating, thereby reducing the frequency of interbreed (prezygotic barrier) or their hybrid offspring maladaptive hybridization (Dobzhansky, 1937; Dobzhan- do not survive or reproduce (post-zygotic barrier). If pre- sky, 1940). This process, known as reinforcement, will and post-zygotic barriers are incomplete, genes from each cause signals used in mate recognition to diverge, thereby reinforcing prezygotic barriers (Sætre et al., 1997b) Correspondence: Jon Haavie, Department of Evolutionary Biology, eventually completing speciation in sympatry. Thus, Evolutionary Biology Centre, Uppsala University, Nordbyva¨gen 18D, SE-752 36 Uppsala, Sweden. depending on the fitness of the hybrid, prezygotic Tel.: +46 18 471 2640; fax: +46 18 471 6310; barriers will either increase or decrease (Parsons et al., e-mail: [email protected] 1993; Sætre et al., 1997b; de Kort et al., 2002). J. EVOL. BIOL. 17 (2004) 227–237 ª 2004 BLACKWELL PUBLISHING LTD 227 228 J. HAAVIE ET AL. Prezygotic barriers are generally assumed to be gen- etically determined (Dobzhansky, 1937). However, pre- mating barriers may develop for nongenetical reasons (Grant & Grant, 1997a). Song in oscine birds is usually learned through an imprinting-like process (Kroodsma, 1982; Catchpole & Slater, 1995). This property may cause song to change rapidly over time and vary geographically (for references see Catchpole & Slater, 1995). It has been suggested that such culturally inherited traits can increase assortative mating and possibly be the starting point for speciation in allopatry (Marler & Tamura, 1962; Baker & Mewaldt, 1978). However, when two closely related species come into secondary contact males may come to copy songs of the wrong model (Helb et al., 1985). Consequently, heterospecific copying may lead to hybridization (Alatalo et al., 1990; Eriksson, 1991; Grant & Grant, 1997c). Whether reinforcement acts on cultu- rally inherited traits to increase assortative mating is largely unknown (Grant & Grant, 1997b). Thus, it is unclear whether culturally inherited traits promote or oppose speciation and the role of song in speciation remains controversial (Raikow, 1986; Baptista & Trail, Fig. 1 The European distribution of the pied flycatcher (grey area) 1992; Salomon & Hemim, 1992; Grant & Grant, 1997a; and collared flycatcher (hatched area). Song recordings are of Irwin & Price, 1999; Irwin et al., 2001; Slabbekoorn & allopatric pied flycatchers from Spain near Madrid (SPA) and Norway Smith, 2002). By comparing traits of populations where near Oslo (NOR), collared flycatchers from Italy in Abruzzo National their distribution overlaps (sympatry) with populations Park (ITA) and Hungary near Budapest (HUN). Sympatric popula- where they live separately (allopatry) we can examine tions of pied and collared flycatchers were from the Baltic island of the effects of coexistence on traits used in species O¨ land, Sweden (SWE) (referred to as the Swedish populations) and recognition. In this way it may be possible to study the Czech Republic in the Jesenı´k mountains (CZE). whether culturally inherited traits promote or oppose speciation. The pied flycatcher (Ficedula hypoleuca, Pall.) and the isolation in a Central European hybrid zone (Sætre et al., collared flycatcher (F. albicollis, Temm.) have overlapping 1997b). The hybrid zone in Central Europe is assumed to breeding distributions in Central and Eastern Europe and be of secondary contact after the Pleistocene glaciations on the Baltic islands of Gotland and O¨ land off the (von Haartman, 1949; Sætre et al., 2001) whereas the Swedish east coast (hereby referred to as the Swedish Swedish hybrid zone is apparently of more recent origin, population) (Fig. 1). They are closely related species with possibly only about 150 years old (Alatalo et al., 1990). genetic distance estimated at approximately 3% at Interestingly, the species differences in male plumage mitochondrial DNA (Sætre et al., 2001). Also, they are characters are more pronounced and the frequency of ecologically very similar as they compete over nest sites hybridization is lower in the Central European than in and territories in sympatry and affect each other’s the Swedish hybrid zone (Alatalo et al., 1994; Sætre et al., population dynamics (Sætre et al., 1999b). The frequency 1999a, 2003). As plumage traits are used in species of hybridization has been estimated at 2–7% in different recognition, this suggests that the prezygotic barriers sympatric populations (Alatalo et al., 1982; Sætre et al., have evolved further in the Central European than in the 1999a; Veen et al., 2001), and hybrids have greatly Swedish hybrid zone (Sætre et al., 1999a). reduced fitness, consistent with Haldane’s rule (Alatalo The songs of the pied and collared flycatcher are et al., 1982; Sætre et al., 1997b, 1999a, 2003). The pied complex, repertoire sizes typically ranging from a few up and the collared flycatcher have a large overlapping to 100 unique song syllables (Lundberg & Alatalo, 1992), breeding distribution (Fig. 1). However, hybridization but easily distinguishable in the field mainly through occurs in a rather narrow zone corresponding to topog- difference in frequency and tempo (Gelter, 1987). In raphy and habitat (Alerstam et al., 1978; Sætre et al., flycatchers, song has been shown to function in territory 1999a). Females of the two species are similar to the defence (Eriksson, 1991) and mate attraction (Eriksson, extent that males of both species are apparently unable to 1986). Females have been shown to base their mate distinguish between them (Sætre et al., 1997a). However, choice on repertoire size (Eriksson, 1991; Lampe & Sætre, female mate choice is not random (Alatalo et al., 1982; 1995) and song activity and complexity has been found Sætre et al., 1997b) and character displacement on male to correlate with the health status and condition of the plumage colour has been found to reinforce premating male (Garamszegi et al., 2003; Lampe & Espmark, 2003). J. EVOL. BIOL. 17 (2004) 227–237 ª 2004 BLACKWELL PUBLISHING LTD Song and reinforcement 229 Both character convergence and divergence have been allopatric collared flycatchers were from Italy (41°49¢N, suggested to occur in the songs of flycatchers. In 13°47¢E) and Hungary (47°43¢N, 19°01¢E) (we classified sympatric populations some pied flycatchers sing a song the Hungarian population as allopatric, but note that the resembling that of the collared flycatcher (Tischler, 1942; pied flycatcher is an occasional, rare breeding bird in this Lo¨ hrl, 1955; Gelter, 1987; Eriksson, 1991), a phenom- area). Sympatric populations were from Sweden enon known as mixed song (Eriksson, 1991). This has (57°10¢N, 16°58¢E) and
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